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Distinctive Patterns of Seizure-Related White Matter Alterations in Right and Left Temporal Lobe Epilepsy

Background: We hypothesized that right and left temporal lobe epilepsy (RTLE and LTLE, respectively) have distinctive spatial patterns of white matter (WM) changes that can be differentiated and interpreted with the use of multiple diffusion parameters. We compared the global microstructure of fiber...

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Autores principales: Buksakowska, Irena, Szabó, Nikoletta, Martinkovič, Lukáš, Faragó, Péter, Király, András, Vrána, Jiří, Kincses, Zsigmond Tamás, Meluzín, Jan, Šulc, Vlastimil, Kynčl, Martin, Roček, Miloslav, Tichý, Michal, Charvát, František, Hořínek, Daniel, Marusič, Petr
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6779711/
https://www.ncbi.nlm.nih.gov/pubmed/31632330
http://dx.doi.org/10.3389/fneur.2019.00986
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author Buksakowska, Irena
Szabó, Nikoletta
Martinkovič, Lukáš
Faragó, Péter
Király, András
Vrána, Jiří
Kincses, Zsigmond Tamás
Meluzín, Jan
Šulc, Vlastimil
Kynčl, Martin
Roček, Miloslav
Tichý, Michal
Charvát, František
Hořínek, Daniel
Marusič, Petr
author_facet Buksakowska, Irena
Szabó, Nikoletta
Martinkovič, Lukáš
Faragó, Péter
Király, András
Vrána, Jiří
Kincses, Zsigmond Tamás
Meluzín, Jan
Šulc, Vlastimil
Kynčl, Martin
Roček, Miloslav
Tichý, Michal
Charvát, František
Hořínek, Daniel
Marusič, Petr
author_sort Buksakowska, Irena
collection PubMed
description Background: We hypothesized that right and left temporal lobe epilepsy (RTLE and LTLE, respectively) have distinctive spatial patterns of white matter (WM) changes that can be differentiated and interpreted with the use of multiple diffusion parameters. We compared the global microstructure of fiber bundles with regard to WM alterations in both RTLE and LTLE, addressing some of the methodological issues of previous studies. Methods: Diffusion tensor imaging data from 17 patients with RTLE (age: 40.7 ± 10.4), 15 patients with LTLE (age: 37.3 ± 10.4), and 15 controls (age: 34.8 ± 11.2) were used in the study. WM integrity was quantified by fractional anisotropy (FA), mean diffusivity (MD), longitudinal diffusivity (LD), and radial diffusivity (RD). The diffusion parameters were compared between the groups in tracts representing the core of the fiber bundles. The volumes of hippocampi and amygdala were subsequently compared across the groups, while the data were adjusted for the effect of hippocampal sclerosis. Results: Significantly reduced FA and increased MD, LD, and RD were found bilaterally over widespread brain regions in RTLE. An increase in MD and RD values was observed in widespread WM fiber bundles ipsilaterally in LTLE, largely overlapping with regions where FA was lower, while no increase in LD was observed. We also found a difference between the LTLE and RTLE groups for the right hippocampal volume (with and without adjustment for HS), whereas no significant volume differences were found between patients and controls. Conclusions: It appears that patients with RTLE exhibit a more widespread pattern of WM alterations that extend far beyond the temporal lobe in both ipsilateral and contralateral hemisphere; furthermore, these changes seem to reflect more severe damage related to chronic degeneration. Conversely, more restrained changes in the LTLE may imply a pattern of less severe axonal damage, more restricted to ipsilateral hemisphere. Comprehensive finding of more prominent hippocampal atrophy in the RTLE raises an interesting issue of seizure-induced implications on gray matter and WM microstructure that may not necessarily mean a straightforward causal relationship. Further correlations of diffusion-derived metrics with neuropsychological and functional imaging measures may provide complementary information on underlying WM abnormalities with regard to functional hemispheric specialization.
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spelling pubmed-67797112019-10-18 Distinctive Patterns of Seizure-Related White Matter Alterations in Right and Left Temporal Lobe Epilepsy Buksakowska, Irena Szabó, Nikoletta Martinkovič, Lukáš Faragó, Péter Király, András Vrána, Jiří Kincses, Zsigmond Tamás Meluzín, Jan Šulc, Vlastimil Kynčl, Martin Roček, Miloslav Tichý, Michal Charvát, František Hořínek, Daniel Marusič, Petr Front Neurol Neurology Background: We hypothesized that right and left temporal lobe epilepsy (RTLE and LTLE, respectively) have distinctive spatial patterns of white matter (WM) changes that can be differentiated and interpreted with the use of multiple diffusion parameters. We compared the global microstructure of fiber bundles with regard to WM alterations in both RTLE and LTLE, addressing some of the methodological issues of previous studies. Methods: Diffusion tensor imaging data from 17 patients with RTLE (age: 40.7 ± 10.4), 15 patients with LTLE (age: 37.3 ± 10.4), and 15 controls (age: 34.8 ± 11.2) were used in the study. WM integrity was quantified by fractional anisotropy (FA), mean diffusivity (MD), longitudinal diffusivity (LD), and radial diffusivity (RD). The diffusion parameters were compared between the groups in tracts representing the core of the fiber bundles. The volumes of hippocampi and amygdala were subsequently compared across the groups, while the data were adjusted for the effect of hippocampal sclerosis. Results: Significantly reduced FA and increased MD, LD, and RD were found bilaterally over widespread brain regions in RTLE. An increase in MD and RD values was observed in widespread WM fiber bundles ipsilaterally in LTLE, largely overlapping with regions where FA was lower, while no increase in LD was observed. We also found a difference between the LTLE and RTLE groups for the right hippocampal volume (with and without adjustment for HS), whereas no significant volume differences were found between patients and controls. Conclusions: It appears that patients with RTLE exhibit a more widespread pattern of WM alterations that extend far beyond the temporal lobe in both ipsilateral and contralateral hemisphere; furthermore, these changes seem to reflect more severe damage related to chronic degeneration. Conversely, more restrained changes in the LTLE may imply a pattern of less severe axonal damage, more restricted to ipsilateral hemisphere. Comprehensive finding of more prominent hippocampal atrophy in the RTLE raises an interesting issue of seizure-induced implications on gray matter and WM microstructure that may not necessarily mean a straightforward causal relationship. Further correlations of diffusion-derived metrics with neuropsychological and functional imaging measures may provide complementary information on underlying WM abnormalities with regard to functional hemispheric specialization. Frontiers Media S.A. 2019-10-01 /pmc/articles/PMC6779711/ /pubmed/31632330 http://dx.doi.org/10.3389/fneur.2019.00986 Text en Copyright © 2019 Buksakowska, Szabó, Martinkovič, Faragó, Király, Vrána, Kincses, Meluzín, Šulc, Kynčl, Roček, Tichý, Charvát, Hořínek and Marusič. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neurology
Buksakowska, Irena
Szabó, Nikoletta
Martinkovič, Lukáš
Faragó, Péter
Király, András
Vrána, Jiří
Kincses, Zsigmond Tamás
Meluzín, Jan
Šulc, Vlastimil
Kynčl, Martin
Roček, Miloslav
Tichý, Michal
Charvát, František
Hořínek, Daniel
Marusič, Petr
Distinctive Patterns of Seizure-Related White Matter Alterations in Right and Left Temporal Lobe Epilepsy
title Distinctive Patterns of Seizure-Related White Matter Alterations in Right and Left Temporal Lobe Epilepsy
title_full Distinctive Patterns of Seizure-Related White Matter Alterations in Right and Left Temporal Lobe Epilepsy
title_fullStr Distinctive Patterns of Seizure-Related White Matter Alterations in Right and Left Temporal Lobe Epilepsy
title_full_unstemmed Distinctive Patterns of Seizure-Related White Matter Alterations in Right and Left Temporal Lobe Epilepsy
title_short Distinctive Patterns of Seizure-Related White Matter Alterations in Right and Left Temporal Lobe Epilepsy
title_sort distinctive patterns of seizure-related white matter alterations in right and left temporal lobe epilepsy
topic Neurology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6779711/
https://www.ncbi.nlm.nih.gov/pubmed/31632330
http://dx.doi.org/10.3389/fneur.2019.00986
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